Resolving genetic functions within microbial populations: In situ analyses using rRNA and mRNA stable isotope probing coupled with single-cell raman-fluorescence in situ hybridizationδ

Applied and Environmental Microbiology

Volumn 75, Issue 1, 2009, Pages 234-241

  Huang, Wei E ^a,f   Ferguson, Andrew ^b,c   Singer, Andrew C ^a   Lawson, Kathryn ^c,d   Thompson, Ian P ^a   Kalin, Robert M ^e   Larkin, Michael J ^c,d   Bailey, Mark J ^a   Whiteley, Andrew S ^a  

^a CENTRE FOR ECOLOGY AND HYDROLOGY   (United Kingdom)

^b Environmental Engineering Research Centre

^c QUESTOR Centre

^d Prifysgol Cymru   (United Kingdom)

^e QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^f UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FLUORESCENCE IN SITU HYBRIDIZATIONS; GROUNDWATER SYSTEMS; IN-SITU; IN-SITU ANALYSIS; MICROBIAL COMMUNITIES; MICROBIAL POPULATIONS; NAPHTHALENE BIODEGRADATIONS; NATURAL ENVIRONMENTS; NATURAL WORLDS; PSEUDOMONAS FLUORESCENS; PSEUDOMONAS SP.; STABLE ISOTOPES;

BIOCHEMISTRY; BIODEGRADATION; BIOMASS; CELL CULTURE; DEGRADATION; ECOLOGY; FLUORESCENCE; FLUORESCENCE MICROSCOPY; FUNCTIONS; GROUNDWATER; HYDROGEOLOGY; INTERNET PROTOCOLS; ISOTOPES; MICROBIOLOGY; MICROORGANISMS; NUCLEIC ACIDS; PROBABILITY DENSITY FUNCTION; RENEWABLE ENERGY RESOURCES; RNA; UNDERGROUND RESERVOIRS;

NAPHTHALENE;

BACTERIUM; BIODEGRADATION; GENETIC ANALYSIS; GROUNDWATER; HYBRIDIZATION; IDENTIFICATION METHOD; MICROBIAL COMMUNITY; STABLE ISOTOPE;

CARBON ISOTOPES; COMAMONADACEAE; DNA, BACTERIAL; IN SITU HYBRIDIZATION, FLUORESCENCE; MOLECULAR SEQUENCE DATA; NAPHTHALENES; PSEUDOMONAS FLUORESCENS; PSEUDOMONAS PUTIDA; RNA, MESSENGER; RNA, RIBOSOMAL; SEQUENCE ANALYSIS, DNA; STAINING AND LABELING; WATER MICROBIOLOGY;

ACIDOVORAX; PROKARYOTA; PSEUDOMONAS; PSEUDOMONAS FLUORESCENS; PSEUDOMONAS SP.;

EID: 58149354855     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01861-08     Document Type: Article

References (45)

1. Amann, R. I., W. Ludwig, and K.-H. Schleifer. 1995. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol. Rev. 59:143-169.
2. Bosch, R., E. Garcia-Valdes, and E. R. B. Moore. 2000. Complete nucleotide sequence and evolutionary significance of a chromosomally encoded naphthalene-degradation lower pathway from Pseudomonas stutzeri AN 10. Gene 245:65-74.
3. Bosch, R., E. Garcia-Valdes, and E. R. B. Moore. 1999. Genetic characterization and evolutionary implications of a chromosomally encoded naphthalene-degradation upper pathway from Pseudomonas stutzeri AN 10. Gene 236:149-157.
4. 15N achieved by disentangling the effects of genome G+C content and isotope enrichment on DNA density. Appl. Environ. Microbiol. 73:3189-3195.
5. Cadisch, G., M. Espana, R. Causey, M. Richter, E. Shaw, J. A. W. Morgan, C. Rahn, and G. D. Bending. 2005. Technical considerations for the use of N-15-DNA stable-isotope probing for functional microbial activity in soils. Rapid Commun. Mass Spectrom. 19:1424-1428.
6. Cane, P. A., and P. A. Williams. 1982. The plasmid-coded metabolism of naphthalene and 2-methylnaphthalene in Pseudomonas strains-phenotypic changes correlated with structural modification of the plasmid Pww60-1. J. Gen. Microbiol. 128:2281-2290.
7. Cebron, A., L. Bodrossy, Y. Chen, A. C. Singer, I. P. Thompson, J. I. Prosser, and J. C. Murrell. 2007. Identity of active methanotrophs in landfill cover soil as revealed by DNA-stable isotope probing. FEMS Microbiol. Ecol. 62:12-23.
8. Daniel, R. 2005. The metagenomics of soil. Nat. Rev. Microbiol. 3:470-478.
9. Dennis, J. J., and G. J. Zylstra. 2004. Complete sequence and genetic organization of pDTG1, the 83 kilobase naphthalene degradation plasmid from Pseudomonas putida strain NCIB 9816-4. J. Mol. Biol. 341:753-768.
10. Ferguson, A. S., W. E. Huang, K. A. Lawson, R. Doherty, O. Gibert, K. W. Dickson, A. S. Whiteley, L. A. Kulakov, I. P. Thompson, R. M. Kalin, and M. J. Larkin. 2007. Microbial analysis of soil and groundwater from a gasworks site and comparison with a sequenced biological reactive barrier remediation process. J. Appl. Microbiol. 102:1227-1238.
11. Gibert, O., A. S. Ferguson, R. M. Kalin, R. Doherty, K. W. Dickso, K. L. McGeough, J. Robinson, and R. Thomas. 2007. Performance of a sequential reactive barrier for bioremediation of coal tar contaminated groundwater. Environ. Sci. Technol. 41:6795-6801.
12. 2)-C-13 pulse labelling of plants in tandem with stable isotope probing: methodological considerations for examining microbial function in the rhizosphere. J. Microbiol. Methods 58:119-129.
13. Huang, W. E., R. I. Griffiths, I. P. Thompson, M. J. Bailey, and A. S. Whiteley. 2004. Raman microscopic analysis of single microbial cells. Anal. Chem. 76:4452-4458.
14. Huang, W. E., K. Stoecker, R. Griffiths, L. Newbold, H. Daims, A. S. Whiteley, and M. Wagner. 2007. Raman-FISH: combining stable-isotope Raman spectroscopy and fluorescence in situ hybridization for the single cell analysis of identity and function. Environ. Microbiol. 9:1878-1889.
15. Huang, W. E., H. Wang, L. F. Huang, H. J. Zheng, A. C. Singer, I. P. Thompson, and A. S. Whiteley. 2005. Chromosomally located gene fusions constructed in Acinetobacter sp. ADP1 for the environmental detection of salicylate. Environ. Microbiol. 7:1339-1348.
16. Kassen, R., and P. B. Rainey. 2004. The ecology and genetics of microbial diversity. Annu. Rev. Microbiol. 58:207-231.
17. Kunapuli, U., T. Lueders, and R. U. Meckenstock. 2007. The use of stable isotope probing to identify key iron-reducing microorganisms involved in anaerobic benzene degradation. ISME J. 1:643-653.
18. Kvist, T., B. K. Ahring, R. S. Lasken, and P. Westermann. 2007. Specific single-cell isolation and genomic amplification of uncultured microorganisms. Appl. Microbiol. Biotechnol. 74:926-935.
19. Larkin, M. J., C. C. R. Allen, L. A. Kulakov, and D. A. Lipscomb. 1999. Purification and characterization of a novel naphthalene dioxygenase from Rhodococcus sp. strain NCIMB12038. J. Bacteriol. 181:6200-6204.
20. Lasken, R. S., and M. Egholm. 2003. Whole genome amplification: abundant supplies of DNA from precious samples or clinical specimens. Trends Biotechnol. 21:531-535.
21. 2)-C-13 pulse-labelling in an upland grassland. Appl. Soil Ecol. 33:152-175.
22. Link, A. J., K. J. Jeong, and G. Georgiou. 2007. Beyond toothpicks: new methods for isolating mutant bacteria. Nat. Rev. Microbiol. 5:680-688.
23. Manefield, M., A. S. Whiteley, R. I. Griffiths, and M. J. Bailey. 2002. RNA stable isotope probing, a novel means of linking microbial community function to phylogeny. Appl. Environ. Microbiol. 68:5367-5373.
24. Marchesi, J. R., f. Sato, A. J. Weightman, T. A. Martin, J. C. Fry, S. J. Hiom, and W. G. Wade. 1998. Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Appl. Environ. Microbiol. 64:795-799.
25. Marcy, Y., T. Ishoey, R. S. Lasken, T. B. Stockwell, B. P. Walenz, A. L. Halpern, K. Y. Beeson, S. M. D. Goldberg, and S. R. Quake. 2007. Nanoliter reactors improve multiple displacement amplification of genomes from single cells. PLoS Genet. 3:1702-1708.
26. McClure, N. C., A. J. Weightman, and J. C. Fry. 1989. Survival of Pseudomonas putida Uwc1 containing cloned catabolic genes in a model activated-sludge unit. Appl. Environ. Microbiol. 55:2627-2634.
27. Morris, S. A., S. Radajewski, T. W. Willison, and J. C. Murrell. 2002. Identification of the functionally active methanotroph population in a peat soil microcosm by stable-isotope probing. Appl. Environ. Microbiol. 68: 1446-1453.
28. Moser, R., and U. Stahl. 2001. Insights into the genetic diversity of initial dioxygenases from PAH-degrading bacteria. Appl. Microbiol. Biotechnol. 55:609-618.
29. Neufeld, J. D., H. Schafer, M. J. Cox, R. Boden, I. R. McDonald, and J. C. Murrell. 2007. Stable-isotope probing implicates Methylophaga spp. and novel gammaproteobacteria in marine methanol and methylamine metabolism. ISME J. 1:480-491.
30. Prinz, C., F. Hook, J. Malm, and P. Sjovall. 2007. Structural effects in the analysis of supported lipid bilayers by time-of-flight secondary ion mass spectrometry. Langmuir 23:8035-8041.
31. Radajewski, S., P. Ineson, N. R. Parekh, and J. C. Murrell. 2000. Stable-isotope probing as a tool in microbial ecology. Nature 403:646-649.
32. Radajewski, S., I. R. McDonald, and J. C. Murrell. 2003. Stable-isotope probing of nucleic acids: a window to the function of uncultured microorganisms. Curr. Opin. Biotechnol. 14:296-302.
33. Raghunathan, A., H. R. Ferguson, C. J. Bornarth, W. M. Song, M. Driscoll, and R. S. Lasken. 2005. Genomic DNA amplification from a single bacterium. Appl. Environ. Microbiol. 71:3342-3347.
34. Schleifer, K.-H. 2004. Microbial diversity: facts, problems and prospects. Syst. Appl. Microbiol. 27:3-9.
35. 18O. Appl. Environ. Microbiol. 73:2541-2546.
36. Simon, M. J., T. D. Osslund, R. Saunders, B. D. Ensley, S. Suggs, A. Harcourt, W. C. Suen, D. L. Cruden, D. T. Gibson, and G. J. Zylstra. 1993. Sequences of genes encoding naphthalene dioxygenase in Pseudomonas putida strains G7 and Ncib-9816-4. Gene 127:31-37.
37. Sogin, M. L., H. G. Morrison, J. A. Huber, D. M. Welch, S. M. Huse, P. R. Neal, J. M. Arrieta, and G. J. Herndl. 2006. Microbial diversity in the deep sea and the underexplored "rare biosphere." Proc. Natl. Acad. Sci. USA 103:12115-12120.
38. Stepanauskas, R., and M. E. Sieracki. 2007. Matching phylogeny and metabolism in the uncultured marine bacteria, one cell at a time. Proc. Natl. Acad. Sci. USA 104:9052-9057.
39. Venter, J. C. 2003. Unleashing the power of genomics: understanding the environment and biological diversity. Scientist 17:8.
40. Venter, J. C., K. Remington, J. F. Heidelberg, A. L. Halpern, D. RUM h. J. A. Eisen, D. Y. Wu, I. Paulsen, K. E. Nelson, W. Nelson, D. E. Fouts, S. Levy, A. H. Knap, M. W. Lomas, K. Nealson, O. White, J. Peterson, J. Hoffman, R. Parsons, H. Baden-Tillson, C. Pfannkoch, Y. H. Rogers, and H. O. Smith. 2004. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66-74.
41. Wang, M. M., E. Tu, D. E. Raymond, J. M. Yang, H. C. Zhang, N. Hagen, B. Dees, E. M. Mercer, A. H. Forster, I. Kariv, P. J. Marchand, and W. F. Butler. 2005. Microfluidic sorting of mammalian cells by optical force switching. Nat. Biotechnol. 23:83-87.
42. Whitman, W. B., D. C. Coleman, and W. J. Wiebe. 1998. Prokaryotes: the unseen majority. Proc. Natl. Acad. Sci. USA 95:6578-6583.
43. Yen, K. M., and C. M. Serdar. 1988. Genetics of naphthalene catabolism in pseudomonads. CRC Crit. Rev. Microbiol. 15:247-268.
44. Zhou, J. Z., M. A. Bruns, and J. M. Tiedje. 1996. DNA recovery from soils of diverse composition. Appl. Environ. Microbiol. 62:316-322.
45. Zhou, N. Y., S. L. Fuenmayor, and P. A. Williams. 2001. nag genes of Ralstonia (formerly Pseudomonas) sp. strain U2 encoding enzymes for gentisate catabolism. J. Bacteriol. 183:700-708.